Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T01:55:30.905Z Has data issue: false hasContentIssue false

Chapter Twelve - Bovine tuberculosis in badgers: sociality, infection and demography in a social mammal

from Part II - Understanding between-host processes

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

Badgers are an important reservoir of bovine TB in the UK. We discuss how the combination of individual epidemiological data, tracking studies and modelling frameworks enabled exploration of host–pathogen theories in relation to badger life history and disease ecology, focusing on heterogeneity in host susceptibility and infectiousness, two components of the superspreader phenotype. Studies pairing empirical data with modelling approaches suggest sex differences are underpinned by immunological mechanisms. We discuss how studies have moved away from the simplistic assumption of randomly mixing homogeneous populations towards recognition of heterogeneity in host association patterns at group, class and individual levels. Interactions between individuals are non-random with high within-group contacts and lower between-group contact rates. Contact heterogeneity is fundamental to understanding what drives/restricts the spatial spread of disease through a population. We explore a demographic perspective on disease ecology, showing how demographic intricacies provide further understanding of the mechanisms underpinning persistence of infected badger populations. The understanding gained from longitudinal studies of host–pathogen field systems is important ecological and epidemiological theory development and informs evidence-based disease control strategies’ development.

Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 342 - 367
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions: I. Regulatory processes. Journal of Animal Ecology, 47, 219247.CrossRefGoogle Scholar
Anderson, R.M. & May, R.M. (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 291, 451524.Google Scholar
Aznar, I., Frankena, K., More, S. J., et al. (2018). Quantification of Mycobacterium bovis transmission in a badger vaccine field trial. Preventive Veterinary Medicine, 149, 2937.CrossRefGoogle Scholar
Beirne, C., Delahay, R., Hares, M. & Young, A. (2014) Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. PLoS ONE, 9, e108964.Google Scholar
Beirne, C., Waring, L., McDonald, R.A., Delahay, R. & Young, A. (2016) Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length. Proceedings of the Royal Society of London B, 283, 20152949.Google Scholar
Benton, C.H., Delahay, R.J., Robertson, A., et al. (2016) Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal. Proceedings of the Royal Society of London B, 283, 20160798.Google Scholar
Blanchong, J.A., Scribner, K.T., Kravchenko, A.N. & Winterstein, S.R. (2007) TB-infected deer are more closely related than non-infected deer. Biology Letters, 3, 104106.CrossRefGoogle ScholarPubMed
Buzdugan, S.N., Vergne, T., Grosbois, V., Delahay, R.J. & Drewe, J.A. (2017) Inference of the infection status of individuals using longitudinal testing data from cryptic populations: towards a probabilistic approach to diagnosis. Scientific Reports, 7, 1111.Google Scholar
Carpenter, P.J., Pope, L.C., Greig, C., et al. (2005) Mating system of the Eurasian badger, Meles meles, in a high density population. Molecular Ecology, 14, 273284.CrossRefGoogle Scholar
Carter, S.P., Chambers, M.A., Rushton, S.P., et al. (2012) BCG vaccination reduces risk of tuberculosis infection in vaccinated badgers and unvaccinated badger cubs. PLoS ONE, 7, e49833.Google Scholar
Carter, S.P., Delahay, R.J., Smith, G.C., et al. (2007) Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology. Proceedings of the Royal Society of London B, 274, 27692777.Google Scholar
Chambers, M.A., Aldwell, F., Williams, G.A., et al. (2017) The effect of oral vaccination with Mycobacterium bovis BCG on the development of tuberculosis in captive European badgers (Meles meles). Frontiers in Cellular and Infection Microbiology, 7(6).Google Scholar
Chambers, M.A., Rogers, F., Delahay, R.J., et al. (2011) Bacillus Calmette–Guérin vaccination reduces the severity and progression of tuberculosis in badgers. Proceedings of the Royal Society of London B, 278, 19131920.Google ScholarPubMed
Cheeseman, C., Wilesmith, J., Stuart, F. & Mallinson, P. (1988) Dynamics of tuberculosis in a naturally infected badger population. Mammal Review, 18, 6172.CrossRefGoogle Scholar
Clifton-Hadley, R., Wilesmith, J. & Stuart, F. (1993) Mycobacterium bovis in the European badger (Meles meles): epidemiological findings in tuberculous badgers from a naturally infected population. Epidemiology and Infection, 111, 919.Google Scholar
Clutton-Brock, T. & Sheldon, B.C. (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution, 25, 562573.Google Scholar
Colchero, F., Jones, O.R. & Rebke, M. (2012) BaSTA: an R package for Bayesian estimation of age‐specific survival from incomplete mark–recapture/recovery data with covariates. Methods in Ecology and Evolution, 3, 466470.Google Scholar
Corner, L.A., O’Meara, D., Costello, E., Lesellier, S. & Gormley, E. (2012) The distribution of Mycobacterium bovis infection in naturally infected badgers. The Veterinary Journal, 194, 166172.CrossRefGoogle ScholarPubMed
Delahay, R., Langton, S., Smith, G., Clifton‐Hadley, R. & Cheeseman, C. (2000) The spatio‐temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high‐density badger population. Journal of Animal Ecology, 69, 428441.Google Scholar
Delahay, R., Walker, N., Forrester, G., et al. (2006) Demographic correlates of bite wounding in Eurasian badgers, Meles meles L., in stable and perturbed populations. Animal Behaviour, 71, 10471055.Google Scholar
Delahay, R., Walker, N., Smith, G., et al. (2013) Long-term temporal trends and estimated transmission rates for Mycobacterium bovis infection in an undisturbed high-density badger (Meles meles) population. Epidemiology and Infection, 141, 14451456.Google Scholar
Donnelly, C.A., Wei, G., Johnston, W.T., et al. (2007) Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. International Journal of Infectious Diseases, 11, 300308.Google Scholar
Donnelly, C.A., Woodroffe, R., Cox, D., et al. (2003) Impact of localized badger culling on tuberculosis incidence in British cattle. Nature, 426, 834837.Google Scholar
Donnelly, C.A., Woodroffe, R., Cox, D., et al. (2006) Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature, 439, 843846.CrossRefGoogle ScholarPubMed
Drewe, J.A., Tomlinson, A.J., Walker, N.J. & Delahay, R.J. (2010) Diagnostic accuracy and optimal use of three tests for tuberculosis in live badgers. PLoS ONE, 5, e11196.CrossRefGoogle ScholarPubMed
Gaillard, J.-M., Festa-Bianchet, M., Yoccoz, N., Loison, A. & Toigo, C. (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics, 31, 367393.CrossRefGoogle Scholar
Gaillard, J., Lemaître, J., Berger, V., et al. (2016) Life history axes of variation. In: The Encyclopedia of Evolutionary Biology (pp. 312323). Oxford: Academic Press.Google Scholar
Gallagher, J. & Clifton-Hadley, R. (2000) Tuberculosis in badgers; a review of the disease and its significance for other animals. Research in Veterinary Science, 69, 203217.Google Scholar
Gallagher, J., Muirhead, R. & Burn, K. (1976) Tuberculosis in wild badgers (Meles meles) in Gloucestershire: pathology. Veterinary Record, 98, 914.Google Scholar
Gallagher, J. & Nelson, J. (1979) Cause of ill health and natural death in badgers in Gloucestershire. Tuberculosis, 10, 1416.Google Scholar
George, S.C., Smith, T.E., Mac Cana, P.S., Coleman, R. & Montgomery, W.I. (2014) Physiological stress in the Eurasian badger (Meles meles): effects of host, disease and environment. General and Comparative Endocrinology, 200, 5460.CrossRefGoogle ScholarPubMed
Graham, A.L., Hayward, A.D., Watt, K.A., et al. (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science, 330, 662665.CrossRefGoogle Scholar
Graham, J., Smith, G., Delahay, R., et al. (2013) Multi-state modelling reveals sex-dependent transmission, progression and severity of tuberculosis in wild badgers. Epidemiology and Infection, 141, 14291436.Google Scholar
Jenkins, H.E., Cox, D. & Delahay, R.J. (2012) Direction of association between bite wounds and Mycobacterium bovis infection in badgers: implications for transmission. PLoS ONE, 7, e45584.Google Scholar
Jenkins, H.E., Morrison, W., Cox, D., et al. (2008) The prevalence, distribution and severity of detectable pathological lesions in badgers naturally infected with Mycobacterium bovis. Epidemiology and Infection, 136, 13501361.Google Scholar
Johnson, P.T., Rohr, J.R., Hoverman, J.T., et al. (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters, 15, 235242.Google Scholar
Joly, D.O., Samuel, M.D., Langenberg, J.A., et al. (2006) Spatial epidemiology of chronic wasting disease in Wisconsin white-tailed deer. Journal of Wildlife Diseases, 42, 578588.Google Scholar
Keeling, M.J. & Danon, L. (2009) Mathematical modelling of infectious diseases. British Medical Bulletin, 92, 3342.Google Scholar
Kelly, G.E., McGrath, G. & More, S.J. (2010) Estimating the extent of spatial association of Mycobacterium bovis infection in badgers in Ireland. Epidemiology and Infection, 138, 270279.CrossRefGoogle ScholarPubMed
Kéry, M. & Schaub, M. (2011) Bayesian Population Analysis Using WinBUGS: A Hierarchical Perspective. New York, NY: Academic Press.Google Scholar
Kramer‐Schadt, S., Fernández, N., Eisinger, D., Grimm, V. & Thulke, H.H. (2009) Individual variations in infectiousness explain long‐term disease persistence in wildlife populations. Oikos, 118, 199208.Google Scholar
Kruuk, L.E. (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359, 873890.Google Scholar
Lebreton, J.D., Nichols, J.D., Barker, R.J., Pradel, R. & Spendelow, J.A. (2009) Modeling individual animal histories with multistate capture–recapture models. Advances in Ecological Research, 41, 87173.Google Scholar
Lesellier, S., Palmer, S., Gowtage-Sequiera, S., et al. (2011) Protection of Eurasian badgers (Meles meles) from tuberculosis after intra-muscular vaccination with different doses of BCG. Vaccine, 29, 37823790.Google Scholar
Lloyd-Smith, J.O., Schreiber, S.J., Kopp, P.E. & Getz, W.M. (2005) Superspreading and the effect of individual variation on disease emergence. Nature, 438, 355359.Google Scholar
Macdonald, D., Harmsen, B., Johnson, P. & Newman, C. (2004) Increasing frequency of bite wounds with increasing population density in Eurasian badgers, Meles meles.Animal Behaviour, 67, 745751.Google Scholar
Macdonald, D.W., Newman, C., Buesching, C.D. & Johnson, P.J. (2008) Male-biased movement in a high-density population of the Eurasian badger (Meles meles). Journal of Mammalogy, 89, 10771086.CrossRefGoogle Scholar
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: Part II. Nature, 280, 455461.Google Scholar
McDonald, J.L., Bailey, T., Delahay, R.J., et al. (2016) Demographic buffering and compensatory recruitment promotes the persistence of disease in a wildlife population. Ecology Letters, 19, 443449.Google Scholar
McDonald, J.L., Robertson, A. & Silk, M.J. (2018) Wildlife disease ecology from the individual to the population: Insights from a long‐term study of a naturally infected European badger population. Journal of Animal Ecology, 87, 101112.CrossRefGoogle Scholar
McDonald, J.L., Smith, G.C., McDonald, R.A., Delahay, R.J. & Hodgson, D. (2014) Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife–disease interactions. Proceedings of the Royal Society of London B, 281, 20140526.Google Scholar
McDonald, R.A., Delahay, R.J., Carter, S.P., Smith, G.C. & Cheeseman, C.L. (2008) Perturbing implications of wildlife ecology for disease control. Trends in Ecology & Evolution, 23, 5356.Google Scholar
Murhead, R.M. & Burns, K.J. (1974) Tuberculosis in wild badgers in Gloucestershire: epidemiology. Veterinary Record, 95, 552555.Google Scholar
Ostfeld, R.S., Levi, T., Jolles, A.E., et al. (2014) Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS ONE, 9, e107387.Google Scholar
Palphramand, K., Delahay, R., Robertson, A., et al. (2017) Field evaluation of candidate baits for oral delivery of BCG vaccine to European badgers, Meles meles. Vaccine, 35, 44024407.Google Scholar
Pfister, C.A. (1998) Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proceedings of the National Academy of Sciences of the United States of America, 95, 213218.Google Scholar
Pradel, R. (2005) Multievent: an extension of multistate capture–recapture models to uncertain states. Biometrics, 61, 442447.CrossRefGoogle ScholarPubMed
Rogers, L., Cheeseman, C., Mallinson, P. & Clifton‐Hadley, R. (1997) The demography of a high‐density badger (Meles meles) population in the west of England. Journal of Zoology, 242, 705728.Google Scholar
Rogers, L., Delahay, R., Cheeseman, C., et al. (1998) Movement of badgers (Meles meles) in a high–density population: individual, population and disease effects. Proceedings of the Royal Society of London B, 265, 12691276.Google Scholar
Roper, T. (2010) Badger (Collins New Naturalist Library, Book 114). London: HarperCollins UK.Google Scholar
Rushmore, J., Caillaud, D., Matamba, L., et al. (2013) Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology, 82, 976986.Google Scholar
Shirley, M.D., Rushton, S.P., Smith, G.C., South, A.B. & Lurz, P.W. (2003) Investigating the spatial dynamics of bovine tuberculosis in badger populations: evaluating an individual-based simulation model. Ecological Modelling, 167, 139157.Google Scholar
Silk, M.J., Croft, D.P., Delahay, R.J., et al. (2017a) Using social network measures in wildlife disease ecology, epidemiology, and management. BioScience, 67, 245257.CrossRefGoogle ScholarPubMed
Silk, M.J., Croft, D.P., Delahay, R.J., et al. (2017b) The application of statistical network models in disease research. Methods in Ecology and Evolution, 8, 10261041.Google Scholar
Sin, Y.W., Annavi, G., Dugdale, H.L., et al. (2014) Pathogen burden, co‐infection and major histocompatibility complex variability in the European badger (Meles meles). Molecular Ecology, 23, 50725088.CrossRefGoogle ScholarPubMed
Smith, G.C., Delahay, R.J., McDonald, R.A. & Budgey, R. (2016) Model of selective and non-selective management of badgers (Meles meles) to control bovine tuberculosis in badgers and cattle. PLoS ONE, 11, e0167206.Google Scholar
Smith, G.C., McDonald, R.A. & Wilkinson, D. (2012) Comparing badger (Meles meles) management strategies for reducing tuberculosis incidence in cattle. PLoS ONE, 7, e39250.Google Scholar
Stearns, S.C. (1983) The influence of size and phylogeny on patterns of covariation among life-history traits in the mammals. Oikos, 41, 173187.Google Scholar
Thrall, P.H., Antonovics, J. & Hall, D.W. (1993) Host and pathogen coexistence in sexually transmitted and vector-borne diseases characterized by frequency-dependent disease transmission. American Naturalist, 142, 543552.Google Scholar
Tomlinson, A., Chambers, M., Carter, S., et al. (2013a) Heterogeneity in the risk of Mycobacterium bovis infection in European badger (Meles meles) cubs. Epidemiology and Infection, 141, 14581466.Google Scholar
Tomlinson, A., Chambers, M. & Delahay, R. (2012) Mycobacterium bovis infection in badger cubs: re-assessing the evidence for maternally derived immunological protection from advanced disease. Veterinary Immunology and Immunopathology, 148, 326330.Google Scholar
Tomlinson, A., Chambers, M., Wilson, G., McDonald, R.A. & Delahay, R. (2013b) Sex‐related heterogeneity in the life‐history correlates of Mycobacterium bovis infection in European badgers (Meles meles). Transboundary and Emerging Diseases, 60, 3745.Google Scholar
Tomlinson, A.J., Chambers, M.A., McDonald, R.A. & Delahay, R.J. (2015) Association of quantitative interferon‐γ responses with the progression of naturally acquired Mycobacterium bovis infection in wild European badgers (Meles meles). Immunology, 144, 263270.Google Scholar
Vicente, J., Delahay, R., Walker, N. & Cheeseman, C. (2007) Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high‐density badger Meles meles population. Journal of Animal Ecology, 76, 348360.Google Scholar
Weber, N., Bearhop, S., Dall, S.R., et al. (2013a) Denning behaviour of the European badger (Meles meles) correlates with bovine tuberculosis infection status. Behavioral Ecology and Sociobiology, 67, 471479.Google Scholar
Weber, N., Carter, S.P., Dall, S.R., et al. (2013b) Badger social networks correlate with tuberculosis infection. Current Biology, 23, R915R916.Google Scholar
Wendland, L.D., Wooding, J., White, C.L., et al. (2010) Social behavior drives the dynamics of respiratory disease in threatened tortoises. Ecology, 91, 12571262.Google Scholar
White, P.C. & Harris, S. (1995) Bovine tuberculosis in badger (Meles meles) populations in southwest England: the use of a spatial stochastic simulation model to understand the dynamics of the disease. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 349, 391413.Google Scholar
Wilkinson, D., Smith, G., Delahay, R. & Cheeseman, C. (2004) A model of bovine tuberculosis in the badger Meles meles: an evaluation of different vaccination strategies. Journal of Applied Ecology, 41, 492501.Google Scholar
Wilkinson, D., Smith, G., Delahay, R., et al. (2000) The effects of bovine tuberculosis (Mycobacterium bovis) on mortality in a badger (Meles meles) population in England. Journal of Zoology, 250, 389395.Google Scholar
Woodroffe, R., Donnelly, C., Johnston, W., et al. (2005) Spatial association of Mycobacterium bovis infection in cattle and badgers Meles meles. Journal of Applied Ecology, 42, 852862.Google Scholar
Woodroffe, R., Donnelly, C.A., Wei, G., et al. (2009) Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). Journal of Animal Ecology, 78, 818827.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×